Biochemistry (Moscow)

, Volume 77, Issue 13, pp 1478–1486 | Cite as

Antisense RNAs as envoys in intercellular communication: 20 years later

Review
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Abstract

More than 20 years ago we showed that some types of cells are capable of secreting RNAs. It was suggested that these secreted RNAs could serve as molecular envoys in intercellular communication, for example, these RNAs being complementary to specific sites of the gene in another cell (e.g. to the variable region of immunoglobulin gene) could regulate the expression of genes that contain sites in coding regions complementary to antisense RNA. It has since been proven that eukaryotic cells contain antisense RNAs (particularly microRNAs and small interfering RNAs), which can regulate the expression of genes at the posttranscriptional level (the so-called regulatory pathway of RNA interference). Here I provide a short review of advances in the field of intracellular regulation of gene expression by different types of RNAs. In addition, an overview of recent data on the secretion of RNA molecules by different cell types and possible involvement of these secreted antisense RNAs in intercellular regulation of gene expression in target cells is given.

Key words

antisense RNA circulating nucleic acids RNA interference gene regulation suppressor T cells secretion intercellular communication 

Abbreviations

cDNA

complementary DNA

dsRNA

double-stranded RNA

esRNA

exosomal shuttle RNA

MHC

major histocompatibility complex

nt

nucleotides

piRNA

piwiRNA

RISC

RNA-induced silencing complex

RNP

ribonucleoproteids

siRNA

small interfering RNA

srRNP

secreted regulatory ribonucleoprotein particles

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References

  1. 1.
    Sitikov, A. S., and Munishkin, A. V. (1991) Dokl. Akad. Nauk SSSR, 318, 1486–1488.PubMedGoogle Scholar
  2. 2.
    Griffith, F. (1928) J. Hyg. (Lond.), 27, 113–159.CrossRefGoogle Scholar
  3. 3.
    Avery, O. T., Macleod, C. M., and McCarty, M. (1994) J. Exp. Med., 79, 137–158.CrossRefGoogle Scholar
  4. 4.
    Watson, J. D., and Crick, F. H. (1953) Cold Spring Harb. Symp. Quant. Biol., 18, 123–131.PubMedCrossRefGoogle Scholar
  5. 5.
    Watson, J. D., and Crick, F. H. (1953) Nature, 171, 964–967.PubMedCrossRefGoogle Scholar
  6. 6.
    Singer, M. F., Jones, O. W., and Nirenberg, M. W. (1963) Proc. Natl. Acad. Sci. USA, 49, 392–399.PubMedCrossRefGoogle Scholar
  7. 7.
    Stroun, M., Anker, P., and Ledoux, L. (1966) Arch. Int. Physiol. Biochim., 74, 935–937.PubMedGoogle Scholar
  8. 8.
    Bendich, A., Wilczok, T., and Borenfreund, E. (1965) Science, 148, 374–376.PubMedCrossRefGoogle Scholar
  9. 9.
    Stroun, M., and Anker, P. (1972) Biochem. J., 128, 100–101.Google Scholar
  10. 10.
    Stroun, M., Anker, P., Maurice, P., and Gahan, P. B. (1977) Int. Rev. Cytol., 51, 1–48.PubMedCrossRefGoogle Scholar
  11. 11.
    Politis, G., Plassara, M. G., and Thomou-Politi, H. (1975) Nature, 257, 485–486.PubMedCrossRefGoogle Scholar
  12. 12.
    Kolodny, G. M. (1971) Exp. Cell Res., 65, 313–324.PubMedCrossRefGoogle Scholar
  13. 13.
    Kolodny, G. M. (1977) Nucleic Acids Res., 4, 271–284.PubMedCrossRefGoogle Scholar
  14. 14.
    Stroun, M., Anker, P., Beljanski, M., Henri, J., Lederrey, C., Ojha, M., and Maurice, P. A. (1969) Cancer Res., 38, 3546–3554.Google Scholar
  15. 15.
    Valentine, F. T., and Lawrence, H. S. (1969) Science, 165, 1014–1016.PubMedCrossRefGoogle Scholar
  16. 16.
    Graybill, J. R., Silva, J., Jr., Alford, R. H., and Thor, D. E. (1973) Cell Immunol., 8, 120–135.PubMedCrossRefGoogle Scholar
  17. 17.
    Khandjian, E. W., and Turian, G. (1976) Cell Differ., 5, 171–188.PubMedCrossRefGoogle Scholar
  18. 18.
    Stroun, M., Anker, P., Maurice, P., and Gahan, P. B. (1977) Int. Rev. Cytol., 51, 1–48.PubMedCrossRefGoogle Scholar
  19. 19.
    Paterson, B. M., Roberts, B. E., and Kuff, E. L. (1977) Proc. Natl. Acad. Sci. USA, 74, 4370–4374.PubMedCrossRefGoogle Scholar
  20. 20.
    Hastie, N. D., and Held, W. A. (1978) Proc. Natl. Acad. Sci. USA, 75, 1217–1221.PubMedCrossRefGoogle Scholar
  21. 21.
    Spencer, C. A., Gietz, R. D., and Hodgetts, R. B. (1986) Nature, 322, 279–281.PubMedCrossRefGoogle Scholar
  22. 22.
    Williams, G. T., Kingston, R., Owen, M. J., Jenkinson, E. J., and Owen, J. J. (1986) Nature, 324, 63–64.PubMedCrossRefGoogle Scholar
  23. 23.
    Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) Cell, 75, 843–854.PubMedCrossRefGoogle Scholar
  24. 24.
    Fire, A., Albertson, D., Harrison, S., and Moerman, D. (1991) Development, 113, 503–514.PubMedGoogle Scholar
  25. 25.
    Guo, S., and Kemphues, K. (1995) Cell, 81, 611–620.PubMedCrossRefGoogle Scholar
  26. 26.
    Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Nature, 391, 806–811.PubMedCrossRefGoogle Scholar
  27. 27.
    Hamilton, A. J., and Baulcombe, D. C. (1999) Science, 286, 950–952.PubMedCrossRefGoogle Scholar
  28. 28.
    Hammond, S. M., Bernstein, E., Beach, D., and Hannon, G. J. (2000) Nature, 404, 293–296.PubMedCrossRefGoogle Scholar
  29. 29.
    Zamore, P. D., Tuschl, T., Sharp, P. A., and Bartel, D. P. (2000) Cell, 101, 25–33.PubMedCrossRefGoogle Scholar
  30. 30.
    Hutvagner, G., and Simard, M. J. (2008) Nat. Rev. Mol. Cell Biol., 9, 22–32.PubMedCrossRefGoogle Scholar
  31. 31.
    Preall, J. B., He, Z., Gorra, J. M., and Sontheimer, E. J. (2006) Curr. Biol., 16, 530–535.PubMedCrossRefGoogle Scholar
  32. 32.
    Kim, V. N., Han, J., and Siomi, M. C. (2009) Nat. Rev. Mol. Cell Biol., 10, 126–139.PubMedCrossRefGoogle Scholar
  33. 33.
    Pritchard, C. C., Cheng, H. H., and Tewari, M. (2012) Nat. Rev. Genet., 13, 358–369.PubMedCrossRefGoogle Scholar
  34. 34.
    Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., and Voinnet, O. (2008) Science, 320, 1185–1190.PubMedCrossRefGoogle Scholar
  35. 35.
    Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R., and Ruvkun, G. (2000) Nature, 403, 901–906.PubMedCrossRefGoogle Scholar
  36. 36.
    Lagos-Quintana, M. (2001) Science, 294, 853–858.PubMedCrossRefGoogle Scholar
  37. 37.
    Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J., and Tuschl, T. (2003) Dev. Cell, 5, 337–350.PubMedCrossRefGoogle Scholar
  38. 38.
    Cox, D. N., Chao, A., and Lin, H. (2000) Development, 127, 503–514.PubMedGoogle Scholar
  39. 39.
    Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V., and Zamore, P. D. (2006) Science, 313, 320–324.PubMedCrossRefGoogle Scholar
  40. 40.
    Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T., Surani, M. A., Sakaki, Y., and Sasaki, H. (2008) Nature, 453, 539–543.PubMedCrossRefGoogle Scholar
  41. 41.
    Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M., and Hannon, G. J. (2008) Nature, 453, 534–538.PubMedCrossRefGoogle Scholar
  42. 42.
    Gantier, M. P., McCoy, C. E., Rusinova, I., Saulep, D., Wang, D., Xu, D., Irving, A. T., Behlke, M. A., Hertzog, P. J., Mackay, F., and Williams, B. R. (2011) Nucleic Acids Res., 39, 5692–5703.PubMedCrossRefGoogle Scholar
  43. 43.
    Zhang, Z., Qin, Y. W., Brewer, G., and Jing, Q. (2012) Wiley Interdiscip. Rev. RNA, 3, 593–600.PubMedCrossRefGoogle Scholar
  44. 44.
    Sijen, T., Steiner, F. A., Thijssen, K. L., and Plasterk, R. H. (2007) Science, 315, 244–247.PubMedCrossRefGoogle Scholar
  45. 45.
    Pak, J., and Fire, A. (2007) Science, 315, 241–244.PubMedCrossRefGoogle Scholar
  46. 46.
    Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A., Timmons, L., Fire, A., and Mello, C. C. (1999) Cell, 99, 123–132.PubMedCrossRefGoogle Scholar
  47. 47.
    Hammond, S. M., Boettcher, S., Caudy, A. A., Kobayashi, R., and Hannon, G. J. (2001) Science, 293, 1146–1150.PubMedCrossRefGoogle Scholar
  48. 48.
    Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H., and Siomi, M. C. (2005) Genes Dev., 19, 2837–2848.PubMedCrossRefGoogle Scholar
  49. 49.
    Rivas, F. V., Tolia, N. H., Song, J. J., Aragon, J. P., Liu, J., Hannon, G. J., and Joshua-Tor, L. (2005) Nat. Struct. Mol. Biol., 12, 340–349.PubMedCrossRefGoogle Scholar
  50. 50.
    Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. (2001) Nature, 409, 363–366.PubMedCrossRefGoogle Scholar
  51. 51.
    Hutvagner, G., McLachlan, J., Pasquinelli, A. E., Balint, E., Tuschl, T., and Zamore, P. D. (2001) Science, 293, 834–838.PubMedCrossRefGoogle Scholar
  52. 52.
    Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M., and Gvozdev, V. A. (2001) Curr. Biol., 11, 1017–1027.PubMedCrossRefGoogle Scholar
  53. 53.
    Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Nature, 411, 494–498.PubMedCrossRefGoogle Scholar
  54. 54.
    Liu, Q., Rand, T. A., Kalidas, S., Du, F., Kim, H. E., Smith, D. P., and Wang, X. (2003) Science, 301, 1921–1925.PubMedCrossRefGoogle Scholar
  55. 55.
    Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., and Kim, V. N. (2003) Nature, 425, 415–419.PubMedCrossRefGoogle Scholar
  56. 56.
    Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G., and Tuschl, T. (2004) Mol. Cell, 15, 185–197.PubMedCrossRefGoogle Scholar
  57. 57.
    Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G., Thomson, J. M., Song, J. J., Hammond, S. M., Joshua-Tor, L., and Hannon, G. J. (2004) Science, 305, 1437–1441.PubMedCrossRefGoogle Scholar
  58. 58.
    Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., Steward, R., and Chen, X. (2005) Science, 307, 932–935.PubMedCrossRefGoogle Scholar
  59. 59.
    Pelisson, A., Sarot, E., Payen-Groschene, G., and Bucheton, A. (2007) J. Virol., 81, 1951–1960.PubMedCrossRefGoogle Scholar
  60. 60.
    Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Cell, 128, 1089–1103.PubMedCrossRefGoogle Scholar
  61. 61.
    Gunawardane, L. S., Saito, K., Nishida, K. M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H., and Siomi, M. C. (2007) Science, 315, 1587–1590.PubMedCrossRefGoogle Scholar
  62. 62.
    Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio-Somoza, I., Leyva, A., Weigel, D., Garcia, J. A., and Paz-Ares, J. (2007) Nat. Genet., 39, 1033–1037.PubMedCrossRefGoogle Scholar
  63. 63.
    Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B. J., Chiang, H. R., King, N., Degnan, B. M., Rokhsar, D. S., and Bartel, D. P. (2008) Nature, 455, 1193–1197.PubMedCrossRefGoogle Scholar
  64. 64.
    Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., Peterson, A., Noteboom, J., O’Briant, K. C., Allen, A., Lin, D. W., Urban, N., Drescher, C. W., Knudsen, B. S., Stirewalt, D. L., Gentleman, R., Vessella, R. L., Nelson, P. S., Martin, D. B., and Tewari, M. (2008) Proc. Natl. Acad. Sci. USA, 105, 10513–10518.PubMedCrossRefGoogle Scholar
  65. 65.
    Pritchard, C. C., Cheng, H. H., and Tewari, M. (2012) Nat. Rev. Genet., 13, 358–369.PubMedCrossRefGoogle Scholar
  66. 66.
    Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., Mitchell, P. S., Bennett, C. F., Pogosova-Agadjanyan, E. L., Stirewalt, D. L., Tait, J. F., and Tewari, M. (2011) Proc. Natl. Acad. Sci. USA, 108, 5003–5008.PubMedCrossRefGoogle Scholar
  67. 67.
    Pan, B. T., and Johnstone, R. M. (1983) Cell, 33, 967–978.PubMedCrossRefGoogle Scholar
  68. 68.
    Johnstone, R. M., Adam, M., Hammond, J. R., Orr, L., and Turbide, C. (1987) J. Biol. Chem., 262, 9412–9420.PubMedGoogle Scholar
  69. 69.
    Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., and Geuze, H. J. (1996) J. Exp. Med., 183, 1161–1172.PubMedCrossRefGoogle Scholar
  70. 70.
    Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G., and Amigorena, S. (1998) Nat. Med., 4, 594–600.PubMedCrossRefGoogle Scholar
  71. 71.
    Lutz, M. B., and Schuler, G. (2002) Trends Immunol., 23, 445–449.PubMedCrossRefGoogle Scholar
  72. 72.
    Peche, H., Heslan, M., Usal, C., Amigorena, S., and Cuturi, M. C. (2003) Transplantation, 76, 1503–1510.PubMedCrossRefGoogle Scholar
  73. 73.
    Quah, B. J., and O’Neill, H. C. (2005) J. Cell Mol. Med., 9, 643–654.PubMedCrossRefGoogle Scholar
  74. 74.
    Van Niel, G., Mallegol, J., Bevilacqua, C., Candalh, C., Brugiere, S., Tomaskovic-Crook, E., Heath, J. K., Cerf-Bensussan, N., and Heyman, M. (2003) Gut, 52, 1690–1697.PubMedCrossRefGoogle Scholar
  75. 75.
    Fevrier, B., and Raposo, G. (2004) Curr. Opin. Cell Biol., 16, 415–421.PubMedCrossRefGoogle Scholar
  76. 76.
    Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., and Raposo, G. (2004) Proc. Natl. Acad. Sci. USA, 101, 9683–9688.PubMedCrossRefGoogle Scholar
  77. 77.
    Mathivanan, S., and Simpson, R. J. (2009) Proteomics, 9, 4997–5000.PubMedCrossRefGoogle Scholar
  78. 78.
    Mathivanan, S., Fahner, C. J., Reid, G. E., and Simpson, R. J. (2012) Nucleic Acids Res., 40, D1241–D1244.PubMedCrossRefGoogle Scholar
  79. 79.
    Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., and Lotvall, J. O. (2007) Nat. Cell Biol., 9, 654–659.PubMedCrossRefGoogle Scholar
  80. 80.
    Thery, C., Ostrowski, M., and Segura, E. (2009) Nat. Rev. Immunol., 9, 581–593.PubMedCrossRefGoogle Scholar
  81. 81.
    Mittelbrunn, M., Gutierrez-Vazquez, C., Villarroya-Beltri, C., Gonzalez, S., Sanchez-Cabo, F., Gonzalez, M. A., Bernad, A., and Sanchez-Madrid, F. (2011) Nat. Commun., 2, 282.PubMedCrossRefGoogle Scholar
  82. 82.
    Batagov, A. O., Kuznetsov, V. A., and Kurochkin, I. V. (2011) BMC Genom., 12,Suppl. 3, S18.CrossRefGoogle Scholar
  83. 83.
    Hu, G., Drescher, K. M., and Chen, X. M. (2012) Front Genet., 3, 56.PubMedGoogle Scholar
  84. 84.
    Pant, S., Hilton, H., and Burczynski, M. E. (2012) Biochem. Pharmacol., 83, 1484–1494.PubMedCrossRefGoogle Scholar
  85. 85.
    Wang, K., Zhang, Z., Weber, J., Baxter, D., and Galas, D. J. (2010) Nucleic Acids Res., 38, 7248–7259.PubMedCrossRefGoogle Scholar
  86. 86.
    Lindstrom, M. S. (2011) Biochem. Res. Int., 2011, 1–16.CrossRefGoogle Scholar
  87. 87.
    Turchinovich, A., Weiz, L., Langheinz, A., and Burwinkel, B. (2011) Nucleic Acids Res., 39, 7223–7233.PubMedCrossRefGoogle Scholar
  88. 88.
    Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., and Remaley, A. T. (2011) Nat. Cell Biol., 13, 423–334.PubMedCrossRefGoogle Scholar
  89. 89.
    Chen, X., Liang, H., Zhang, J., Zen, K., and Zhang, C. Y. (2012) Protein Cell, 3, 28–37.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  1. 1.Northwestern UniversityChicagoUSA

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